In Situ Coral Nurseries Serve as Genetic Repositories for Coral Reef Restoration after an Extreme Cold‐Water Event

During an unusual cold‐water event in January 2010, reefs along the Florida Reef Tract suffered extensive coral mortality, especially in shallow reef habitats in close proximity to shore and with connections to coastal bays. The threatened staghorn coral, Acropora cervicornis, is the focus of propagation and restoration activities in Florida and one of the species that exhibited high susceptibility to low temperatures. Complete mortality of wild staghorn colonies was documented at 42.9% of donor sites surveyed after the cold event. Remarkably, 72.7% of sites with complete A. cervicornis mortality had fragments surviving within in situ coral nurseries. Thus, coral nurseries served as repositories for genetic material that would have otherwise been completely lost from donor sites. The location of the coral nurseries at deeper habitats and distanced from shallow nearshore habitats that experienced extreme temperature conditions buffered the impacts of the cold‐water event and preserved essential local genotypes for future Acropora restoration activities.     

Turbid reefs moderate coral bleaching under climate‐related temperature stress

Thermal‐stress events that cause coral bleaching and mortality have recently increased in frequency and severity. Yet few studies have explored conditions that moderate coral bleaching. Given that high light and high ocean temperature together cause coral bleaching, we explore whether corals at turbid localities, with reduced light, are less likely to bleach during thermal‐stress events than corals at other localities. We analyzed coral bleaching, temperature, and turbidity data from 3,694 sites worldwide with a Bayesian model and found that K_d490, a measurement positively related to turbidity, between 0.080 and 0.127 reduced coral bleaching during thermal‐stress events. Approximately 12% of the world's reefs exist within this “moderating turbidity” range, and 30% of reefs that have moderating turbidity are in the Coral Triangle. We suggest that these turbid nearshore environments may provide some refuge through climate change, but these reefs will need high conservation status to sustain them close to dense human populations.     

Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments

Studying the mechanisms that enable coral populations to inhabit spatially varying thermal environments can help evaluate how they will respond in time to the effects of global climate change and elucidate the evolutionary forces that enable or constrain adaptation. Inshore reefs in the Florida Keys experience higher temperatures than offshore reefs for prolonged periods during the summer. We conducted a common garden experiment with heat stress as our selective agent to test for local thermal adaptation in corals from inshore and offshore reefs. We show that inshore corals are more tolerant of a 6‐week temperature stress than offshore corals. Compared with inshore corals, offshore corals in the 31 °C treatment showed significantly elevated bleaching levels concomitant with a tendency towards reduced growth. In addition, dinoflagellate symbionts (Symbiodinium sp.) of offshore corals exhibited reduced photosynthetic efficiency. We did not detect differences in the frequencies of major (>5%) haplotypes comprising Symbiodinium communities hosted by inshore and offshore corals, nor did we observe frequency shifts (‘shuffling’) in response to thermal stress. Instead, coral host populations showed significant genetic divergence between inshore and offshore reefs, suggesting that in Porites astreoides, the coral host might play a prominent role in holobiont thermotolerance. Our results demonstrate that coral populations inhabiting reefs <10‐km apart can exhibit substantial differences in their physiological response to thermal stress, which could impact their population dynamics under climate change.     

Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event

Documenting successional dynamics of coral communities following large-scale bleaching events is necessary to predict coral population responses to global climate change. In 1998, high sea surface temperatures and low cloud cover in the western Pacific Ocean caused high coral mortality on the outer exposed reefs of Palau (Micronesia), while coral mortality in sheltered bays was low. Recovery was examined from 2001 to 2005 at 13 sites stratified by habitat (outer reefs, patch reefs and bays) and depth (3 and 10 m). Two hypotheses were tested: (1) rates of change of coral cover vary in accordance with habitat, and (2) recovery rates depend on recruitment. Coral cover increased most in the sheltered bays, despite a low recruitment rate, suggesting that recovery in bays was primarily a consequence of remnant regrowth. Recruitment densities were consistently high on the wave-exposed reefs, particularly the western slopes, where recovery was attributed to both recruitment and regrowth of remnants. Recovery was initially more rapid at 10 m than 3 m on outer reefs, but in 2004, recovery rates were similar at both depths. Rapid recovery was possible because Palau’s coral reefs were buffered by remnant survival and recruitment from the less impacted habitats.     

Mass Coral Bleaching in 2010 in the Southern Caribbean

Ocean temperatures are increasing globally and the Caribbean is no exception. An extreme ocean warming event in 2010 placed Tobago''s coral reefs under severe stress resulting in widespread coral bleaching and threatening the livelihoods that rely on them. The bleaching response of four reef building taxa was monitored over a six month period across three major reefs systems in Tobago. By identifying taxa resilient to bleaching we propose to assist local coral reef managers in the decision making process to cope with mass bleaching events. The bleaching signal (length of exposure to high ocean temperatures) varied widely between the Atlantic and Caribbean reefs, but regardless of this variation most taxa bleached. Colpophyllia natans, Montastraea faveolata and Siderastrea siderea were considered the most bleaching vulnerable taxa. Interestingly, reefs with the highest coral cover showed the greatest decline reef building taxa, and conversely, reefs with the lowest coral cover showed the most bleaching but lowest change in coral cover with little algal overgrowth post-bleaching.     

Susceptibility of central Red Sea corals during a major bleaching event

A major coral bleaching event occurred in the central Red Sea near Thuwal, Saudi Arabia, in the summer of 2010, when the region experienced up to 10–11 degree heating weeks. We documented the susceptibility of various coral taxa to bleaching at eight reefs during the peak of this thermal stress. Oculinids and agaricids were most susceptible to bleaching, with up to 100 and 80 % of colonies of these families, respectively, bleaching at some reefs. In contrast, some families, such as mussids, pocilloporids, and pectinids showed low levels of bleaching (<20 % on average). We resurveyed the reefs 7 months later to estimate subsequent mortality. Mortality was highly variable among taxa, with some taxa showing evidence of full recovery and some (e.g., acroporids) apparently suffering nearly complete mortality. The unequal mortality among families resulted in significant change in community composition following the bleaching. Significant factors in the likelihood of coral bleaching during this event were depth of the reef and distance of the reef from shore. Shallow reefs and inshore reefs had a higher prevalence of bleaching. This bleaching event shows that Red Sea reefs are subject to the same increasing pressures that reefs face worldwide. This study provides a quantitative, genus-level assessment of the vulnerability of various coral groups from within the Red Sea to bleaching and estimates subsequent mortality. As such, it can provide valuable insights into the future for reef communities in the Red Sea.     

Larval connectivity across temperature gradients and its potential effect on heat tolerance in coral populations

Coral reefs are increasingly exposed to elevated temperatures that can cause coral bleaching and high levels of mortality of corals and associated organisms. The temperature threshold for coral bleaching depends on the acclimation and adaptation of corals to the local maximum temperature regime. However, because of larval dispersal, coral populations can receive larvae from corals that are adapted to very different temperature regimes. We combine an offline particle tracking routine with output from a high‐resolution physical oceanographic model to investigate whether connectivity of coral larvae between reefs of different thermal regimes could alter the thermal stress threshold of corals. Our results suggest that larval transport between reefs of widely varying temperatures is likely in the Coral Triangle and that accounting for this connectivity may be important in bleaching predictions. This has important implications in conservation planning, because connectivity may allow some reefs to have an inherited heat tolerance that is higher or lower than predicted based on local conditions alone.     

Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.     

Global assessment of coral bleaching and required rates of adaptation under climate change

Elevated ocean temperatures can cause coral bleaching, the loss of colour from reef‐building corals because of a breakdown of the symbiosis with the dinoflagellate Symbiodinium. Recent studies have warned that global climate change could increase the frequency of coral bleaching and threaten the long‐term viability of coral reefs. These assertions are based on projecting the coarse output from atmosphere–ocean general circulation models (GCMs) to the local conditions around representative coral reefs. Here, we conduct the first comprehensive global assessment of coral bleaching under climate change by adapting the NOAA Coral Reef Watch bleaching prediction method to the output of a low‐ and high‐climate sensitivity GCM. First, we develop and test algorithms for predicting mass coral bleaching with GCM‐resolution sea surface temperatures for thousands of coral reefs, using a global coral reef map and 1985–2002 bleaching prediction data. We then use the algorithms to determine the frequency of coral bleaching and required thermal adaptation by corals and their endosymbionts under two different emissions scenarios. The results indicate that bleaching could become an annual or biannual event for the vast majority of the world's coral reefs in the next 30–50 years without an increase in thermal tolerance of 0.2–1.0°C per decade. The geographic variability in required thermal adaptation found in each model and emissions scenario suggests that coral reefs in some regions, like Micronesia and western Polynesia, may be particularly vulnerable to climate change. Advances in modelling and monitoring will refine the forecast for individual reefs, but this assessment concludes that the global prognosis is unlikely to change without an accelerated effort to stabilize atmospheric greenhouse gas concentrations.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

Caribbean massive corals not recovering from repeated thermal stress events during 2005–2013

Massive coral bleaching events associated with high sea surface temperatures are forecast to become more frequent and severe in the future due to climate change. Monitoring colony recovery from bleaching disturbances over multiyear time frames is important for improving predictions of future coral community changes. However, there are currently few multiyear studies describing long‐term outcomes for coral colonies following acute bleaching events. We recorded colony pigmentation and size for bleached and unbleached groups of co‐located conspecifics of three major reef‐building scleractinian corals (Orbicella franksi, Siderastrea siderea, and Stephanocoenia michelini; n = 198 total) in Bocas del Toro, Panama, during the major 2005 bleaching event and then monitored pigmentation status and changes live tissue colony size for 8 years (2005–2013). Corals that were bleached in 2005 demonstrated markedly different response trajectories compared to unbleached colony groups, with extensive live tissue loss for bleached corals of all species following bleaching, with mean live tissue losses per colony 9 months postbleaching of 26.2% (±5.4 SE) for O. franksi, 35.7% (±4.7 SE) for S. michelini, and 11.2% (±3.9 SE) for S. siderea. Two species, O. franksi and S. michelini, later recovered to net positive growth, which continued until a second thermal stress event in 2010. Following this event, all species again lost tissue, with previously unbleached colony species groups experiencing greater declines than conspecific sample groups, which were previously bleached, indicating a possible positive acclimative response. However, despite this beneficial effect for previously bleached corals, all groups experienced substantial net tissue loss between 2005 and 2013, indicating that many important Caribbean reef‐building corals will likely suffer continued tissue loss and may be unable to maintain current benthic coverage when faced with future thermal stress forecast for the region, even with potential benefits from bleaching‐related acclimation.     

Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching

The disruption of the coral–algae symbiosis (coral bleaching) due to rising sea surface temperatures has become an unprecedented global threat to coral reefs. Despite decades of research, our ability to manage mass bleaching events remains hampered by an incomplete mechanistic understanding of the processes involved. In this study, we induced a coral bleaching phenotype in the absence of heat and light stress by adding sugars. The sugar addition resulted in coral symbiotic breakdown accompanied by a fourfold increase of coral‐associated microbial nitrogen fixation. Concomitantly, increased N:P ratios by the coral host and algal symbionts suggest excess availability of nitrogen and a disruption of the nitrogen limitation within the coral holobiont. As nitrogen fixation is similarly stimulated in ocean warming scenarios, here we propose a refined coral bleaching model integrating the cascading effects of stimulated microbial nitrogen fixation. This model highlights the putative role of nitrogen‐fixing microbes in coral holobiont functioning and breakdown.     

Nearshore coral growth declining on the Mesoamerican Barrier Reef System

Anthropogenic global change and local stressors are impacting coral growth and survival worldwide, altering the structure and function of coral reef ecosystems. Here, we show that skeletal extension rates of nearshore colonies of two abundant and widespread Caribbean corals (Siderastrea siderea, Pseudodiploria strigosa) declined across the Belize Mesoamerican Barrier Reef System (MBRS) over the past century, while offshore coral conspecifics exhibited relatively stable extension rates over the same temporal interval. This decline has caused nearshore coral extension rates to converge with those of their historically slower growing offshore coral counterparts. For both species, individual mass coral bleaching events were correlated with low rates of skeletal extension within specific reef environments, but no single bleaching event was correlated with low skeletal extension rates across all reef environments. We postulate that the decline in skeletal extension rates for nearshore corals is driven primarily by the combined effects of long‐term ocean warming and increasing exposure to higher levels of land‐based anthropogenic stressors, with acute thermally induced bleaching events playing a lesser role. If these declining trends in skeletal growth of nearshore S. siderea and P. strigosa continue into the future, the structure and function of these critical nearshore MBRS coral reef systems is likely to be severely impaired.     

Coral reef resilience to thermal stress in the Eastern Tropical Pacific

Coral reefs worldwide are threatened by thermal stress caused by climate change. Especially devastating periods of coral loss frequently occur during El Niño‐Southern Oscillation (ENSO) events originating in the Eastern Tropical Pacific (ETP). El Niño‐induced thermal stress is considered the primary threat to ETP coral reefs. An increase in the frequency and intensity of ENSO events predicted in the coming decades threatens a pan‐tropical collapse of coral reefs. During the 1982–1983 El Niño, most reefs in the Galapagos Islands collapsed, and many more in the region were decimated by massive coral bleaching and mortality. However, after repeated thermal stress disturbances, such as those caused by the 1997–1998 El Niño, ETP corals reefs have demonstrated regional persistence and resiliency. Using a 44 year dataset (1970–2014) of live coral cover from the ETP, we assess whether ETP reefs exhibit the same decline as seen globally for other reefs. Also, we compare the ETP live coral cover rate of change with data from the maximum Degree Heating Weeks experienced by these reefs to assess the role of thermal stress on coral reef survival. We find that during the period 1970–2014, ETP coral cover exhibited temporary reductions following major ENSO events, but no overall decline. Further, we find that ETP reef recovery patterns allow coral to persist under these El Niño‐stressed conditions, often recovering from these events in 10–15 years. Accumulative heat stress explains 31% of the overall annual rate of change of living coral cover in the ETP. This suggests that ETP coral reefs have adapted to thermal extremes to date, and may have the ability to adapt to near‐term future climate‐change thermal anomalies. These findings for ETP reef resilience may provide general insights for the future of coral reef survival and recovery elsewhere under intensifying El Niño scenarios.     

Thermal stress induces persistently altered coral reef fish assemblages

Ecological communities are reorganizing in response to warming temperatures. For continuous ocean habitats this reorganization is characterized by large‐scale species redistribution, but for tropical discontinuous habitats such as coral reefs, spatial isolation coupled with strong habitat dependence of fish species imply that turnover and local extinctions are more significant mechanisms. In these systems, transient marine heatwaves are causing coral bleaching and profoundly altering habitat structure, yet despite severe bleaching events becoming more frequent and projections indicating annual severe bleaching by the 2050s at most reefs, long‐term effects on the diversity and structure of fish assemblages remain unclear. Using a 23‐year time series spanning a thermal stress event, we describe and model structural changes and recovery trajectories of fish communities after mass bleaching. Communities changed fundamentally, with the new emergent communities dominated by herbivores and persisting for >15 years, a period exceeding realized and projected intervals between thermal stress events on coral reefs. Reefs which shifted to macroalgal states had the lowest species richness and highest compositional dissimilarity, whereas reefs where live coral recovered exceeded prebleaching fish richness, but remained dissimilar to prebleaching compositions. Given realized and projected frequencies of bleaching events, our results show that fish communities historically associated with coral reefs will not re‐establish, requiring substantial adaptation by managers and resource users.     

Boring sponges,an increasing threat for coral reefs affected by bleaching events

Coral bleaching is a stress response of corals induced by a variety of factors, but these events have become more frequent and intense in response to recent climate‐change‐related temperature anomalies. We tested the hypothesis that coral reefs affected by bleaching events are currently heavily infested by boring sponges, which are playing a significant role in the destruction of their physical structure. Seventeen reefs that cover the entire distributional range of corals along the Mexican Pacific coast were studied between 2005/2006, and later between 2009/2010. Most of these coral reefs were previously impacted by bleaching events, which resulted in coral mortalities. Sponge abundance and species richness was used as an indicator of bioerosion, and coral cover was used to describe the present condition of coral reefs. Coral reefs are currently highly invaded (46% of the samples examined) by a very high diversity of boring sponges (20 species); being the coral reef framework the substrate most invaded (56%) followed by the rubbles (45%), and the living colonies (36%). The results also indicated that boring sponges are promoting the dislodgment of live colonies and large fragments from the framework. In summary, the eastern coral reefs affected by bleaching phenomena, mainly provoked by El Niño, present a high diversity and abundance of boring sponges, which are weakening the union of the colony with the reef framework and promoting their dislodgment. These phenomena will probably become even more intense and severe, as temperatures are projected to continue to rise under the scenarios for future climate change, which could place many eastern coral reefs beyond their survival threshold.     

The effects of sea surface temperature anomalies on oceanic coral reef systems in the southwestern tropical Atlantic

In 2010, high sea surface temperatures that were recorded in several parts of the world and caused coral bleaching and coral mortality were also recorded in the southwest Atlantic Ocean, between latitudes 0°S and 8°S. This paper reports on coral bleaching and diseases in Rocas Atoll and Fernando de Noronha archipelago and examines their relationship with sea surface temperature (SST) anomalies recorded by PIRATA buoys located at 8°S30°W, 0°S35°W, and 0°S23°W. Adjusted satellite data were used to derive SST climatological means at buoy sites and to derive anomalies at reef sites. The whole region was affected by the elevated temperature anomaly that persisted through 2010, reaching 1.67 °C above average at reef sites and 1.83 °C above average at buoys sites. A significant positive relationship was found between the percentage of coral bleaching that was observed on reef formations and the corresponding HotSpot SST anomaly recorded by both satellite and buoys. These results indicate that the warming observed in the ocean waters was followed by a warming at the reefs. The percentage of bleached corals persisting after the subsidence of the thermal stress, and disease prevalence increased through 2010, after two periods of thermal stress. The in situ temperature anomaly observed during the 2009–2010 El Niño event was equivalent to the anomaly observed during the 1997–1998 El Niño event, explaining similar bleaching intensity. Continued monitoring efforts are necessary to further assess the relationship between bleaching severity and PIRATA SST anomalies and improve the use of this new dataset in future regional bleaching predictions.     

Spatial and temporal genetic structure of Symbiodinium populations within a common reef‐building coral on the Great Barrier Reef

The dinoflagellate photosymbiont Symbiodinium plays a fundamental role in defining the physiological tolerances of coral holobionts, but little is known about the dynamics of these endosymbiotic populations on coral reefs. Sparse data indicate that Symbiodinium populations show limited spatial connectivity; however, no studies have investigated temporal dynamics for in hospite Symbiodinium populations following significant mortality and recruitment events in coral populations. We investigated the combined influences of spatial isolation and disturbance on the population dynamics of the generalist Symbiodinium type C2 (ITS1 rDNA) hosted by the scleractinian coral Acropora millepora in the central Great Barrier Reef. Using eight microsatellite markers, we genotyped Symbiodinium in a total of 401 coral colonies, which were sampled from seven sites across a 12‐year period including during flood plume–induced coral bleaching. Genetic differentiation of Symbiodinium was greatest within sites, explaining 70–86% of the total genetic variation. An additional 9–27% of variation was explained by significant differentiation of populations among sites separated by 0.4–13 km, which is consistent with low levels of dispersal via water movement and historical disturbance regimes. Sampling year accounted for 6–7% of total genetic variation and was related to significant coral mortality following severe bleaching in 1998 and a cyclone in 2006. Only 3% of the total genetic variation was related to coral bleaching status, reflecting generally small (8%) reductions in allelic diversity within bleached corals. This reduction probably reflected a loss of genotypes in hospite during bleaching, although no site‐wide changes in genetic diversity were observed. Combined, our results indicate the importance of disturbance regimes acting together with limited oceanographic transport to determine the genetic composition of Symbiodinium types within reefs.     

New insights into global patterns of ocean temperature anomalies: implications for coral reef health and management

Aim Coral reefs are widely considered to be particularly vulnerable to changes in ocean temperatures, yet we understand little about the broad‐scale spatio‐temporal patterns that may cause coral mortality from bleaching and disease. Our study aimed to characterize these ocean temperature patterns at biologically relevant scales. Location Global, with a focus on coral reefs. Methods We created a 4‐km resolution, 21‐year global ocean temperature anomaly (deviations from long‐term means) database to quantify the spatial and temporal characteristics of temperature anomalies related to both coral bleaching and disease. Then we tested how patterns varied in several key metrics of disturbance severity, including anomaly frequency, magnitude, duration and size. Results Our analyses found both global variation in temperature anomalies and fine‐grained spatial variability in the frequency, duration and magnitude of temperature anomalies. However, we discovered that even during major climatic events with strong spatial signatures, like the El Niño–Southern Oscillation, areas that had high numbers of anomalies varied between years. In addition, we found that 48% of bleaching‐related anomalies and 44% of disease‐related anomalies were less than 50 km², much smaller than the resolution of most models used to forecast climate changes. Main conclusions The fine‐scale variability in temperature anomalies has several key implications for understanding spatial patterns in coral bleaching‐ and disease‐related anomalies as well as for designing protected areas to conserve coral reefs in a changing climate. Spatial heterogeneity in temperature anomalies suggests that certain reefs could be targeted for protection because they exhibit differences in thermal stress. However, temporal variability in anomalies could complicate efforts to protect reefs, because high anomalies in one year are not necessarily predictive of future patterns of stress. Together, our results suggest that temperature anomalies related to coral bleaching and disease are likely to be highly heterogeneous and could produce more localized impacts of climate change.